Escape by inking and secreting: marine molluscs avoid predators through a rich array of chemicals and mechanisms

Inking by marine molluscs such as sea hares, cuttlefish, squid, and octopuses is a striking behavior that is ideal for neuroecological explorations. While inking is generally thought to be used in active defense against predators, experimental evidence for this view is either scant or lacks mechanistic explanations. Does ink act through the visual or chemical modality? If inking is a chemical defense, how does it function and how does it affect the chemosensory systems of predators? Does it facilitate escape not only by acting directly on predators but also by being an alarm signal for conspecifics? This review examines these issues, within a broader context of passive and active chemical defensive secretions. It focuses on recent work on mechanisms of defense by inking in sea hares (Aplysia) and extends what we have learned about sea hares to other molluscs including the cephalopods.     

Sea hares use novel antipredatory chemical defenses

Numerous studies have demonstrated that chemical defenses protect prey from predation and have often assumed that these defenses function by repelling predators. Surprisingly, few have investigated the mechanisms whereby predators are affected by these defenses. Here, we examine mechanisms of chemical defense of sea hares (Aplysia californica), which, when attacked by spiny lobsters (Panulirus interruptus), release defensive secretions from ink and opaline glands. We show that ink-opaline facilitates the escape of sea hares by acting through a combination of novel and conventional mechanisms. Ink-opaline contains millimolar quantities of amino acids that stimulate chemoreceptor neurons in the spiny lobster's nervous system. Ink stimulates appetitive and ingestive behavior, opaline can elicit appetitive behavior but can also inhibit ingestion and evoke escape responses, and both stimulate grooming. These results suggest that these secretions function by "phagomimicry," in which ink-opaline stimulates the feeding pathway to deceive spiny lobsters into attending to a false food stimulus, and by sensory disruption, in which the sticky and potent secretions cause high-amplitude, long-lasting chemo-mechanosensory stimulation. In addition, opaline contains a chemical deterrent that opposes appetitive effects. Thus, chemical defenses may act in more complex manners than palatability assays of prey chemistry may suggest.     

Overview of the chemical ecology of benthic marine invertebrates along the western Antarctic peninsula

Thirteen years ago in a review that appeared in the American Zoologist, we presented the first survey of the chemical and ecological bioactivity of Antarctic shallow-water marine invertebrates. In essence, we reported that despite theoretical predictions to the contrary the incidence of chemical defenses among sessile and sluggish Antarctic marine invertebrates was widespread. Since that time we and others have significantly expanded upon the base of knowledge of Antarctic marine invertebrates' chemical ecology, both from the perspective of examining marine invertebrates in new, distinct geographic provinces, as well as broadening the evaluation of the ecological significance of secondary metabolites. Importantly, many of these studies have been framed within established theoretical constructs, particularly the Optimal Defense Theory. In the present article, we review the current knowledge of chemical ecology of benthic marine invertebrates comprising communities along the Western Antarctic Peninsula (WAP), a region of Antarctica that is both physically and biologically distinct from the rest of the continent. Our overview indicates that, similar to other regions of Antarctica, anti-predator chemical defenses are widespread among species occurring along the WAP. In some groups, such as the sponges, the incidence of chemical defenses against predation is comparable to, or even slightly higher than, that found in tropical marine systems. While there is substantial knowledge of the chemical defenses of benthic marine invertebrates against predators, much less is known about chemical anti-foulants. The sole survey conducted to date suggests that secondary metabolites in benthic sponges are likely to be important in the prevention of fouling by benthic diatoms, yet generally lack activity against marine bacteria. Our understanding of the sensory ecology of Antarctic benthic marine invertebrates, despite its great potential, remains in its infancy. For example, along the WAP, community-level non-consumptive effects occur when amphipods chemically sense fish predators and respond by seeking refuge in chemically-defended macroalgae. Such interactions may be important in releasing amphipods from predation pressure and facilitating their unusually high abundances along the WAP. Moreover, recent studies on the sensory biology of the Antarctic keystone sea star Odontaster validus indicate that chemotactile-mediated interactions between conspecifics and other sympatric predatory sea stars may have significant ramifications in structuring community dynamics. Finally, from a global environmental perspective, understanding how chemical ecology structures marine benthic communities along the WAP must increasingly be viewed in the context of the dramatic impacts of rapid climatic change now occurring in this biogeographic region.     

Feeding repellence of Antarctic and sub-Antarctic benthic invertebrates against the omnivorous sea star Odontaster validus

Antarctic and sub-Antarctic benthic invertebrates are subjected to intense predation by mobile macroinvertebrates. Accordingly, chemical protection as well as other defensive mechanisms are expected to be common in organisms inhabiting these ecosystems. In order to evaluate anti-predation activities and allocation of chemical defenses within the anatomy of marine benthic Antarctic and sub-Antarctic invertebrates, 55 species were tested for feeding repellence against the sea star Odontaster validus, a common eurybathic sympatric predator. The invertebrates tested were collected from the deep waters of two poorly surveyed areas in terms of chemical ecology studies: the eastern Weddell Sea (Antarctica) and the vicinities of Bouvet Island (sub-Antarctica). Experiments were conducted at the Spanish Antarctic Base in Deception Island. In the feeding deterrence experiments, shrimp pieces were treated with crude lipophilic fractions obtained from each species, and were offered to the sea stars. A total of 29 species (53 %) from 7 different phyla (Porifera, Cnidaria, Chordata, Bryozoa, Echinodermata, Mollusca, and Annelida) showed feeding repellence against O. validus, and are therefore chemically protected against this keystone predator. Furthermore, 25 species were dissected into parts to investigate the possible allocation of defensive compounds. Some of the results obtained from these analyses support the prediction that the most exposed/vulnerable tissues concentrate chemical defenses to avoid predation against the sea stars. In summary, the results obtained in our survey support the hypothesis that deep-water Antarctic and sub-Antarctic benthic invertebrates are well protected chemically against sympatric predators, similarly to what has been reported in previous studies investigating shallow-water Antarctic species.     

Chemical defenses: from compounds to communities

Marine natural products play critical roles in the chemical defense of many marine organisms and in some cases can influence the community structure of entire ecosystems. Although many marine natural products have been studied for biomedical activity, yielding important information about their biochemical effects and mechanisms of action, much less is known about ecological functions. The way in which marine consumers perceive chemical defenses can influence their health and survival and determine whether some natural products persist through a food chain. This article focuses on selected marine natural products, including okadaic acid, brevetoxins, lyngbyatoxin A, caulerpenyne, bryostatins, and isocyano terpenes, and examines their biosynthesis (sometimes by symbiotic microorganisms), mechanisms of action, and biological and ecological activity. We selected these compounds because their impacts on marine organisms and communities are some of the best-studied among marine natural products. We discuss the effects of these compounds on consumer behavior and physiology, with an emphasis on neuroecology. In addition to mediating a variety of trophic interactions, these compounds may be responsible for community-scale ecological impacts of chemically defended organisms, such as shifts in benthic and pelagic community composition. Our examples include harmful algal blooms; the invasion of the Mediterranean by Caulerpa taxifolia; overgrowth of coral reefs by chemically rich macroalgae and cyanobacteria; and invertebrate chemical defenses, including the role of microbial symbionts in compound production.     

Does concentrating chemical defenses within specific regions of marine sponges result in enhanced protection from predators?

Chemical defenses are an effective mode of predator deterrence across benthic marine organisms, but their production may come with associated costs to the organism as limited resources are diverted away from primary processes like growth and reproduction. Organisms concentrating ecologically relevant levels of these defenses in tissues most at risk to predator attack may alleviate this cost while deterring predators. We addressed this hypothesis by investigating the deterrence of chemical extracts from the inner and outer regions of the sponges Aplysina fulva, Ircinia felix, and I. campana from a temperate hard-bottom reef in the South Atlantic Bight. Assays were conducted using natural fish assemblages and sea urchins. Although, A. fulva and I. felix have higher concentrations of defensive metabolites in the outer and inner regions, respectively, extracts from these regions did not display enhanced deterrency against fish or mobile invertebrate predators. Likewise, extracts from both regions of the sponge Ircinia campana, which has a uniform distribution of defensive chemicals throughout, did not differ in their ability to deter either group of predators. Since chemical defenses were effective deterrents at lower concentrations, secondary metabolite allocation patterns observed among these sponges are likely not driven by predation pressure from generalist fish and mobile invertebrate predators on these reefs. Alternatively, these patterns may be driven by other ecological stressors, another suite of predators, or may be more effective at deterring predators when combined with structural defenses.     

Acidity enhances the effectiveness of active chemical defensive secretions of sea hares, <Emphasis Type="Italic">Aplysia californica</Emphasis>, against spiny lobsters, <Emphasis Type="Italic">Panulirus interruptus</Emphasis>

Sea hares such as Aplysia californica, gastropod molluscs lacking a protective shell, can release a purple cloud of chemicals when vigorously attacked by predators. This active chemical defense is composed of two glandular secretions, ink and opaline, both of which contain an array of compounds. This secretion defends sea hares against predators such as California spiny lobsters Panulirus interruptus via multiple mechanisms, one of which is phagomimicry, in which secretions containing feeding chemicals attract and distract predators toward the secretion and away from the sea hare. We show here that ink and opaline are highly acidic, both having a pH of ∼5. We examined if the acidity of ink and opaline affects their phagomimetic properties. We tested behavioral and electrophysiological responses of chemoreceptor neurons in the olfactory and gustatory organs of P. interruptus, to ink and opaline of A. californica within their natural range of pH values, from ∼5 to 8. Both behavioral and electrophysiological responses to ink and opaline were enhanced at low pH, and low pH alone accounted for most of this effect. Our data suggest that acidity enhances the phagomimetic chemical defense of sea hares.     

Marine chemical ecology: what''s known and what''s next?

In this review, I summarize recent developments in marine chemical ecology and suggest additional studies that should be especially productive. Direct tests in both the field and laboratory show that secondary metabolites commonly function as defenses against consumers. However, some metabolites also diminish fouling, inhibit competitors or microbial pathogens, and serve as gamete attractants; these alternative functions are less thoroughly investigated. We know little about how consumers perceive secondary metabolites or how ecologically realistic doses of defensive metabolites affect consumer physiology or fitness, as opposed to feeding behavior. Secondary metabolites have direct consequences, but they do not act in isolation from other prey characteristics or from the physical and biological environment in which organisms interact with their natural enemies. This mandates that marine chemical ecology be better integrated into a broader and more complex framework that includes aspects of physiological, population, community, and even ecosystem ecology. Recent advances in this area involve assessing how chemically mediated interactions are affected by physical factors such as flow, desiccation, UV radiation, and nutrient availability, or by biological forces such as the palatability or defenses of neighbors, fouling organisms, or microbial symbionts. Chemical defenses can vary dramatically among geographic regions, habitats, individuals within a local habitat, and within different portions of the same individual. Factors affecting this variance are poorly known, but include physical stresses and induction due to previous attack. Studies are needed to assess which consumers induce prey defenses, how responses vary in environments with differing physical characteristics, and whether the ‘induced’ responses are a direct response to consumer attack or are a defense against microbial pathogens invading via feeding wounds. Although relatively unstudied, ontogenetic shifts in concentrations and types of defenses occur in marine species, and patterns of larval chemical defenses appear to provide insights into the evolution of complex life cycles and of differing modes of development among marine invertebrates. The chemical ecology of marine microbes is vastly underappreciated even though microbes produce metabolites that can have devastating indirect effects on non-target organisms (e.g., red tide related fish kills) and significantly affect entire ecosystems. The natural functions of these metabolites are poorly understood, but they appear to deter both consumers and other microbes. Additionally, marine macro-organisms use metabolites from microbial symbionts to deter consumers, subdue prey, and defend their embryos from pathogens. Microbial chemical ecology offers unlimited possibilities for investigators that develop rigorous and more ecologically relevant approaches.     

Temporal environmental variation and phenotypic plasticity: a mechanism underlying priority effects

Understanding the role of history in the formation of communities has been a major challenge in community ecology. Here, we explore the role of phenotypic plasticity and its associated trait‐mediated indirect interactions as a mechanism behind priority effects. Using organisms with inducible defenses as a model system, we examine how aquatic communities initially containing different predator environments are affected at the individual and community level by the colonization of a second predator. Snails and tadpoles were established in four different caged‐predator environments (no predator, fish, crayfish or water bugs). These four communities were then crossed with three predator colonization treatments (no colonization, early colonization, or late colonization) using lethal water bugs as the predator. The snails responded to the caged predator environments with predator‐specific behavioral and morphological defenses. In the colonization treatments, snails possessing the wrong phenotype attempted to induce phenotypic changes to defend themselves against the new risk. However, snails initially induced by a different predator environment often suffered high predation rates. Hence, temporal variation in predation risk not only challenged the snail prey to try to track this environmental variation through time by adjusting their defensive phenotypes, but also caused trait‐mediated interactions between snails and the colonizing predator. For tadpoles within these communities, there was little evidence that the morphological responses of snails indirectly effected tadpole predation rates by colonizing water bugs. Unexpectedly, predation rates on tadpoles by colonizing water bugs were generally higher in the three caged‐predator treatments, suggesting that water bugs elevated their foraging activity in response to potentially competing predators. In summary, we demonstrate an important priority effect in which the initial occurrence of one species of predator can facilitate predation by a second predator that colonizes at a later date (i.e. a TMII) suggesting that phenotypic plasticity can be an important driver behind priority effects (i.e. historical exposure to predators).     

The peril of the plankton

The pelagic environment is characterized by unevenly distributed resources and risks. Such unpredictability presents adaptive challenges to diverse planktonic organisms including the larvae of benthic marine invertebrates. Estimates of mortality during planktonic development are highly variable, ranging from 0% to 100% per day. Predation is considered a significant source of this mortality, but what explains the variability in estimates of the mortality of marine invertebrate larvae? While differential exposure of larval prey to predators may explain these widely variable estimates, adaptations that reduce vulnerability of marine larvae to predators may also be important. Although there are excellent reviews of predation upon larvae and of larval mortality and defenses, nearly 15 years have elapsed since these topics were formally reviewed. Here, we highlight recent advances in understanding the behavioral, chemical, and morphological defenses that larvae possess and assess their effectiveness in reducing the risk of predation. While recent work confirms that larval mortality is generally high, it also demonstrates that larvae can reduce their risk of predation in several ways, including: (1) temporarily escaping the benthos during vulnerable early stages, (2) producing chemical compounds that reduce palatability, (3) possessing morphological defenses such as spines and shells, and (4) exhibiting induced defensive responses whereby larvae can alter their behavior, morphology, and life histories in the presence of predators. Taken together, these studies indicate that marine invertebrate larvae possess a sophisticated suite of defensive phenotypes that have allowed them to persist in the life cycle of benthic invertebrates for eons.     

Influence of proximal stimuli on swimming in the sea hare Aplysia brasiliana

Although the neurobiology and physiology of sea hares are extensively studied, comparatively little is known about their behaviour or ecology. Several species of sea hares swim, but the function of swimming is unclear. In this paper, we tested the hypotheses that swimming in Aplysia brasiliana serves to find food and mates, and to escape predators. Our data strongly support the hypothesis that swimming in A. brasiliana is related to feeding. Sea hares deprived of food overnight swam 12 times longer than ones that had been fed. When sea hares contacted food while swimming they invariably stopped, while those contacting a plastic algal mimic mostly continued to swim. Our experiments provided no evidence to support the hypothesis that swimming in sea hares is related to social behaviour. Sea hares deprived of copulatory mates for 3 days did not swim longer than ones held in copulating groups. Moreover, swimming sea hares never stopped swimming upon encountering a conspecific. Our experiments also supported the hypothesis that swimming in sea hares is related to predation. Sea hares stimulated with a standardised tail pinch and exposed to ink of conspecifics swam four times longer than control individuals, and tail-pinched sea hares that released ink swam five times longer than ones that did not release ink. However, because predators of adult sea hares are mostly lacking and because sea hares often swim spontaneously without predators being present, we conclude that swimming behaviour in A. brasiliana is primarily related to food-finding.     

Multiple components in ink of the sea hare Aplysia californica are aversive to the sea anemone Anthopleura sola

Sea hares of the genus Aplysia rely on an array of behavioral and chemical defenses, including the release of ink and opaline, to protect themselves from predation. While many studies have demonstrated that ink and opaline are repellent to predators, very little is known about which components of these secretions are active against predators. Ink was previously shown to facilitate the escape of Aplysia from predatory anemones (Anthopleura) by eliciting tentacle retraction and/or shriveling, and gastrovascular eversion, but the metabolites mediating this interaction were not identified. We investigated the metabolites in Aplysia californica secretions that were aversive to the anemone Anthopleura sola, as demonstrated by tentacle shriveling and/or retraction. We found that ink elicited tentacle shriveling and/or retraction, while opaline elicited a feeding response. The active components in ink do not appear to be diet-dependent, as ink was aversive regardless of diet (natural seaweed diet vs. Gracilaria ferox). Furthermore, metabolites extracted from G. ferox were not aversive, suggesting that the aversive components are produced by the sea hares. We then examined escapin, a protein in ink with antimicrobial properties. Escapin quickly forms reaction products when mixed with the amino acids l-lysine and l-arginine, which would occur when ink and opaline are released into the sea hare mantle cavity. Neither escapin alone nor escapin mixed with its amino acid substrate l-lysine elicited aversive behaviors either immediately before or 2 min before applying to the tentacles. In addition, escapin mixed with opaline and applied to tentacles after 2 min did not elicit a significant aversive response. Using bioassay-guided fractionation, we attempted to isolate the components in A. californica ink that are aversive to A. sola. We determined that multiple components in ink, including both lipophilic and hydrophilic constituents, elicited aversive responses. We hypothesize that these components may facilitate A. californica's escape from A. sola by eliciting tentacle shriveling and/or retraction, which lead to anemones dropping ensnared sea hares.     

How do predators cope with chemically defended foods?

Many prey species (including plants) deter predators with defensive chemicals. These defensive chemicals act by rendering the prey's tissues noxious, toxic, or both. Here, I explore how predators cope with the presence of these chemicals in their diet. First, I describe the chemosensory mechanisms by which predators (including herbivores) detect defensive chemicals. Second, I review the mechanisms by which predators either avoid or tolerate defensive chemicals in prey. Third, I examine how effectively free-ranging predators can overcome the chemical defenses of prey. The available evidence indicates that predators have mixed success overcoming these defenses. This conclusion is based on reports of free-ranging predators rejecting unpalatable but harmless prey, or voluntarily ingesting toxic prey.     

Marine biofilm bacteria evade eukaryotic predation by targeted chemical defense

Many plants and animals are defended from predation or herbivory by inhibitory secondary metabolites, which in the marine environment are very common among sessile organisms. Among bacteria, where there is the greatest metabolic potential, little is known about chemical defenses against bacterivorous consumers. An emerging hypothesis is that sessile bacterial communities organized as biofilms serve as bacterial refuge from predation. By testing growth and survival of two common bacterivorous nanoflagellates, we find evidence that chemically mediated resistance against protozoan predators is common among biofilm populations in a diverse set of marine bacteria. Using bioassay-guided chemical and genetic analysis, we identified one of the most effective antiprotozoal compounds as violacein, an alkaloid that we demonstrate is produced predominately within biofilm cells. Nanomolar concentrations of violacein inhibit protozoan feeding by inducing a conserved eukaryotic cell death program. Such biofilm-specific chemical defenses could contribute to the successful persistence of biofilm bacteria in various environments and provide the ecological and evolutionary context for a number of eukaryote-targeting bacterial metabolites.     

Evidence of weaker phenotypic plasticity by prey to novel cues from non‐native predators

A central question in evolutionary biology is how coevolutionary history between predator and prey influences their interactions. Contemporary global change and range expansion of exotic organisms impose a great challenge for prey species, which are increasingly exposed to invading non‐native predators, with which they share no evolutionary history. Here, we complete a comprehensive survey of empirical studies of coevolved and naive predator?prey interactions to assess whether a shared evolutionary history with predators influences the magnitude of predator‐induced defenses mounted by prey. Using marine bivalves and gastropods as model prey, we found that coevolved prey and predator‐naive prey showed large discrepancies in magnitude of predator‐induced phenotypic plasticity. Although naive prey, predominantly among bivalve species, did exhibit some level of plasticity – prey exposed to native predators showed significantly larger amounts of phenotypic plasticity. We discuss these results and the implications they may have for native communities and ecosystems.     

Taste-mediated behavioral and electrophysiological responses by the predatory fish Ariopsis felis to deterrent pigments from Aplysia californica ink

Chemical defenses are used by many organisms to avoid predation, and these defenses may function by stimulating predators’ chemosensory systems. Our study examined detection mechanisms for components of defensive ink of sea hares, Aplysia californica, by predatory sea catfish, Ariopsis felis. Behavioral analyses show aplysioviolin and phycoerythrobilin are detected intra-orally and by barbels and are deterrent at concentrations as low as 0.1% full strength. We performed electrophysiological recordings from the facial–trigeminal nerve complex innervating the maxillary barbel and tested aplysioviolin, phycoerythrobilin, amino acids, and bile salts in cross-adaptation experiments. Amino acids and bile salts are known stimulatory compounds for teleost taste systems. Our results show aplysioviolin and phycoerythrobilin are equally stimulatory and completely cross-adapt to each other’s responses. Adaptation to aplysioviolin or phycoerythrobilin reduced but did not eliminate responses to amino acids or bile salts. Adaptation to amino acids or bile salts incompletely reduced responses to aplysioviolin or phycoerythrobilin. The fact that cross-adaptations with aplysioviolin and phycoerythrobilin were not completely reciprocal indicates there are amino acid and bile salt sensitive fibers insensitive to aplysioviolin and phycoerythrobilin. These results indicate two gustatory pathways for aplysioviolin and phycoerythrobilin: one independent of amino acids and bile salts and another shared with some amino acids.     

Low‐pH seawater alters indirect interactions in rocky‐shore tidepools

Ocean acidification is expected to degrade marine ecosystems, yet most studies focus on organismal‐level impacts rather than ecological perturbations. Field studies are especially sparse, particularly ones examining shifts in direct and indirect consumer interactions. Here we address such connections within tidepool communities of rocky shores, focusing on a three‐level food web involving the keystone sea star predator, Pisaster ochraceus, a common herbivorous snail, Tegula funebralis, and a macroalgal basal resource, Macrocystis pyrifera. We demonstrate that during nighttime low tides, experimentally manipulated declines in seawater pH suppress the anti‐predator behavior of snails, bolstering their grazing, and diminishing the top‐down influence of predators on basal resources. This attenuation of top‐down control is absent in pools maintained experimentally at higher pH. These findings suggest that as ocean acidification proceeds, shifts of behaviorally mediated links in food webs could change how cascading effects of predators manifest within marine communities.     

Vulnerability of sea hares to fish predators: importance of diet and fish species

Many sea hares (Opisthobranchia, Anaspidea) sequester secondary metabolites from their algal diets. Tests of the hypothesis that sequestered metabolites deter predators have yielded ambiguous results. We manipulated secondary metabolites in vivo by collecting the sea hare Stylocheilus striatus from different host algae, and by raising it in the laboratory on artificial diets containing or lacking secondary metabolites (malyngamides A and B). Sea hares were then offered to fish. Fish identity affected vulnerability of sea hares to predation far more than did diet history. Wrasses and bream ate most sea hares tasted; damselfishes, goatfishes, and other fishes rejected most. Diet history affected vulnerability of sea hares to wrasses in one of four experiments, and if data from all experiments were pooled, but the effect was modest. Diet history did not affect vulnerability of sea hares to other fish taxa. Despite several studies, evidence for diet-derived defenses against predators in sea hares remains equivocal.     

Responses of the sea catfish Ariopsis felis to chemical defenses from the sea hare Aplysia californica

Ink secretion of sea hares (Aplysia spp.), which is a mixture of co-released ink from the ink gland and opaline from the opaline gland, protects sea hares from predatory invertebrates through diverse mechanisms. These include both aversive or deterrent compounds and also high concentrations of amino acids that stimulate the predators' chemical senses and divert the attack through phagomimicry or sensory disruption. The aim of the present study was to examine if sea hares also defend themselves from predatory vertebrates by interacting with their chemical senses. We used sea catfish, Ariopsis felis, in behavioral and electrophysiological experiments. Behavioral tests on sea catfish show that ink is aversive: when ink is added to palatable food items (noodles with food flavoring), the noodles are no longer eaten, and when ink is added to noodles without food flavoring, the noodles are avoided more than unflavored noodles. Behavioral tests also show that opaline and the amino acid components of either opaline or ink are appetitive. Electrophysiological recordings of chemosensory neuronal activity in the olfactory epithelium and maxillary barbels show that the olfactory and gustatory systems of sea catfish are highly stimulated by ink and opaline, and that the amino acid components of ink and opaline significantly contribute to these responses. Compounds generated by the activity of escapin, an L-amino acid oxidase in the secretion, are moderately stimulatory to both olfactory and gustatory systems. Taken together, our results support the idea that sea hares are chemically defended from predatory sea catfish largely through unpalatable chemical deterrents in ink, but possibly also through amino acids stimulating olfactory and gustatory systems and thus functioning through phagomimicry or sensory disruption.     

Neuroecology, chemical defense, and the keystone species concept

Neuroecology unifies principles from diverse disciplines, scaling from biophysical properties of nerve and muscle cells to community-wide impacts of trophic interactions. Here, these principles are used as a common fabric, woven from threads of chemosensory physiology, behavior, and population and community ecology. The "keystone species" concept, for example, is seminal in ecological theory. It defines a species whose impacts on communities are far greater than would be predicted from its relative abundance and biomass. Similarly, neurotoxins could function in keystone roles. They are rare within natural habitats but exert strong effects on species interactions at multiple trophic levels. Effects of two guanidine alkaloids, tetrodotoxin (TTX) and saxitoxin (STX), coalesce neurobiological and ecological perspectives. These molecules compose some of the most potent natural poisons ever described, and they are introduced into communities by one, or only a few, host species. Functioning as voltage-gated sodium channel blockers for nerve and muscle cells, TTX and STX serve in chemical defense. When borrowed by resistant consumer species, however, they are used either in chemical defense against higher order predators or for chemical communication as chemosensory excitants. Cascading effects of the compounds profoundly impact community-wide attributes, including species compositions and rates of material exchange. Thus, a diverse array of physiological traits, expressed differentially across many species, renders TTX and STX fully functional as keystone molecules, with vast ecological consequences at multiple trophic levels.